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Egg banks in hypersaline lakes of the South-East Europe

Salvatore Moscatello and Genuario Belmonte*
Address: Laboratory of Zoogeography and Fauna, Department of Biological and Environmental Sciences and Technologies, University of Salento,
Via Prov.le Lecce-Monteroni, 73100 Lecce, Italy
Email: Salvatore Moscatello - salvatore.moscatello@virgilio.it; Genuario Belmonte* - genuario.belmonte@unisalento.it
* Corresponding author

Published: 17 March 2009

Saline Systems 2009, 5:3

doi:10.1186/1746-1448-5-3

Received: 17 September 2008

Accepted: 17 March 2009

This article is available from: http://www.salinesystems.org/content/5/1/3

2009 Moscatello and Belmonte; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract
The cyst banks of 6 coastal hypersaline lakes of South-East Europe have been investigated. The
study concerned the bottom sediments of Khersonesskoe and Koyashskoe lakes in the Crimea
(Ukraine), Nart saltworks (Albania), Vecchia Salina at Torre Colimena (Apulia, Italy), Pantano
Grande and Pantano Roveto at Vendicari (Sicily, Italy). A total of 19 cyst types were recognised.
The cyst banks of lakes were found to be well separated in the representation derived from a
statistical multivariate data analysis. For all the lakes examined a comparison was possible between
the resting community in sediments (cyst bank) and the active one in the water. The cyst banks
contained more species than those recorded over a multi-year sampling effort in the water column.
The study of cyst hatching, performed on 5 cyst types under lab conditions, demonstrated that
cysts do not hatch under the same conditions. Furthermore, each cyst type shows a wide range of
preferential hatching conditions, which allow us to confirm the ecological generalism of salt lake
species.

Background
Hypersaline lakes have been stimulating the interest of
biologists for a long time, principally on account of their
simple biological composition [1]. Over the last decades,
the scientific literature on salt lakes has grown with the
appearance of a large number of papers, and new research
directions, e.g. ecology of hypersaline environments [2],
agriculture applied to saline lakes [3], and saline lake conservation and management [4]. Recently, research on
saline lake species assemblages has developed in scope
and intensity. A general rule on the composition of biological communities has been recognised with an inverse
correlation existing between species richness and salinity
[1], with a small number of trophic roles each represented
by just one species [5]. The species composition differs in
saline waters of different chemistry [6,7], being characterized by marine originated fauna with Artemia shrimps

where Cl-1 anions where dominant, and by non marine

Calanoida copepods (family Diaptomidae) where SO4-2 is
the main anion.
Thanks to the ability of many species to produce resting
stages, coupled with long lasting periods of lacking of suitable conditions for active populations, hypersaline lakes
hide a potential biodiversity (in terms of dormant species)
which cannot be investigated by collecting organisms
only from the water column. In fact, commonly during
both dry-hot and freezing-cold seasons, most species stay
in a dormant stage in the bottom sediments. The rest
could even last for years if suitable conditions do not
return (e.g. in the case of progressively rising salinity), giving a progressive reduction of active biodiversity (as in the
case of the Aral Sea, see [8]). In these cases only a small
portion of the biodiversity is expressed, the majority of

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species being temporarily resting as cysts in the sediments.

Even on the return of suitable conditions, only a portion
of the cysts produced will hatch, while the other ones go
to storage the persistent cyst bank, where they can remain
viable for decades or longer [9]. A recent study [10] demonstrated that the number of cyst types in the sediment of
a salt lake were more than those of organisms present in
the water (and carefully studied with a year round sample
effort).
In studies carried out on cyst banks, generally most viable
(responsive) cysts occur in the upper centimetres,
although variations occur along the sediment column
[11]. The accumulation of cysts of different species, generations and genotypes with variable germination rates,
results in a complex assemblage which supplies the active
community, representing the resilience of each system
and the core of the so-called Supply Vertical Ecology [12].
Some recent opinions stress the opportunity to adopt
integrated investigation procedures (collecting both from
the water column and from the sediments) to obtain
information as complete as possible on the species composition of a periodically stressed environment [10,13].
Based on these points, sampling stations for long-term
observation of biology and correlated variables (meteorology and hydrology) could be established in key hypersaline lakes to integrate data with geographic information
with the aim to monitor changes in saline lake areas [4].
This paper aims to spread the practice of the cyst bank
analysis in geographically extended investigations on the
biodiversity of water bodies. In fact the great advantage
that the cyst bank analysis offers reducing the sampling
effort would be carefully considered in geographically
extended studies. In addition, any studies on resting stages
will add information for the understanding of population
dynamics of hypersaline plankters, leading to a significant
improvement of our knowledge of the basic functioning
of hypersaline lake systems.

Results
A total of 19 cyst morphotypes were found (only 13 are
given in Figure 1) in the 6 hypersaline lakes studied. Seven
of them have been identified at the genus level, also due
to the successful hatching experiments carried out in laboratory conditions. On the average, the number of cyst
morphotypes extracted from the sediment cores was more
than double the number of the active organisms found in
the plankton over the study time [see Additional file 1].
The richest cyst bank was that of Vecchia Salina (17 morphotypes), and the poorest was that of lake Koyashskoe (5
morphotypes).
The most common cyst types were Turbellaria cocoons,
which were present in all the sediment samples. Regard-

Figure stages
Resting
sediment
1 of the(cysts)
studied
of hypersaline
plankton organisms
lakes collected in the
Resting stages (cysts) of plankton organisms collected in the sediment of the studied hypersaline
lakes. In some groups the outer sculpturing may help in
taxon identification: a) resting eggs of large branchiopods (a1
Phallocryptus spinosa; a2 Artemia parthenogenetica) (range 200
400 m); b) ephippium of anomopod cladocerans (Moina
salina) holding one resting egg (range 0,51 mm); c) types of
spherical resting eggs in calanoid copepods (range 80200
m); d) types of monogonont rotifers resting eggs (d2 Hexarthra fennica; d3 Brachionus sp.; d4 Ptygura sp.)(range 80200
m); (e) flask-shaped cyst in ciliates (Fabrea salina) (range 80
200 m); f) undetermined spherical resting eggs (range 80
200 m); g) type of spherical resting eggs in turbellarians
(range 80200 m).

ing abundances, the cyst bank of lake Pantano Grande at

Vendicari (Sicily, Italy) was the richest, and Koyashskoe
was the poorest (average on three multilayered cores from
each lake, 10812 and 504 cysts/100 cm3 respectively).
Generally the cyst content in upper sediment layers was
higher than that in the lower ones, but in the Vecchia
Salina (Apulia, Italy) the difference among the three layers
considered (03, 36, and 69 cm) was not evident
(3924, 2634, and 3284 cysts/100 cm3 respectively) and in
Khersonesskoe the trend was reversed (4747, 4937, and
6088 cysts/100 cm3) (Figure 2).
Some species as Moina salina (Cladocera), Artemia urmiana
[14] and Artemia sp. (Anostraca) were exclusive of deeper
layers in the lakes studied. The cyst assemblage composiPage 2 of 7
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The SIMPER procedure associated with MDS of all samples identified the main species responsible for the biotic
characterisation of each lake [see Additional file 2].
Artemia sp. eggs characterised the "cyst bank" of Nart saltworks (SIMPER, similarity percentage: 73%), A. urmiana
eggs characterised the Koyashskoe lake (SIMPER, similarity percentage: 69%), Copepoda Calanoida eggs (unidentified) and Hexarthra fennica eggs characterised the
Khersonesskoe lake (SIMPER, similarity percentage:
84%), while Turbellaria cocoons and Hexarthra fennica
eggs were the main responsible for the average similarity
of Vecchia Salina, Pantano Grande and Pantano Roveto in
Italy (SIMPER, similarity percentage: 72%, 70% and 75%,
respectively).
3=
at
KHE
dicari
pond
KOY
Figure
Vendicari
=
(Apulia,
=(Sicily,
Khersonesskoe
Koyashskoe
2 of(Sicily,
Italy);
Italy);
TCL
lake
Italy);
NRT
lake
(Crimean
=PRV
=sediment
(Crimean
Torre
Nart
); Pantano
PGR
Colimena
saltworks
Peninsula,
Peninsula,
= Pantano
Roveto
(Vlor,
Ukraine)
pool
Grande
Albania);
Salina)
at Venpool
Abundance
lakes
(number
cysts
of cysts/100
in
the
cm
layers
of(Vecchia
theUkraine);
investigated
Abundance of cysts in the sediment layers of the
investigated lakes (number of cysts/100 cm3); PGR =
Pantano Grande pool at Vendicari (Sicily, Italy); PRV
= Pantano Roveto pool at Vendicari (Sicily, Italy); TCL
= Torre Colimena (Vecchia Salina) pond (Apulia,
Italy); NRT = Nart saltworks (Vlor, Albania); KHE
= Khersonesskoe lake (Crimean Peninsula, Ukraine);
KOY = Koyashskoe lake (Crimean Peninsula,
Ukraine).

tion demonstrated highly significant differences among

lakes (ANOSIM, R value = 0,947, P***). This result is
clearly shown by MDS plot (Figure 3): samples (represented by cyst types and abundances) from each hypersaline lake grouped separately one another.

Laboratory experiments under controlled conditions let

us to estimate the hatching success of some species (Figure
4). In Fabrea salina (Ciliophora) 100% of hatching was
obtained in equinox conditions (12 h light, 12 h dark; at
a salinity of 46 after 1 week). In Hexarthra fennica
(Rotifera) the maximum hatching (93%) was obtained in
summer light conditions (14 h light; 10 h dark; at a salinity of 46 after 2 weeks). In Brachionus sp. (Rotifera) a
hatching peak (66,7%) occurred after 3 days at a salinity
of 46, under summer light conditions. Artemia sp.
(Crustacea Anostraca) showed the maximum hatchingrate under summer conditions (67% at a salinity of 36
after 3 days). Moina salina (Crustacea Cladocera) showed
an hatching peak (70%) occurring at a salinity of 26
after 2 weeks, in summer light conditions.

Discussion and conclusion

The study of cyst bank of 6 hypersaline lakes allowed us to
give a dimension to the unexpressed, potential biodiversity inhabiting such a typology of stressed environments.
A sensible portion of the biodiversity of each lake rests
during most of the year, and only a portion of the species
present result active in the water column at each date. The
accumulation of cysts of different species, generations and
genotypes with variable hatching rates leads to a mixed
cyst bank more bio-diverse than the active community
sampled at any one moment.

Figure
MDS
"seed
plot
banks"
3 showing
from the
differences
studied of
lakes
cyst composition among
MDS plot showing differences of cyst composition
among "seed banks" from the studied lakes. The absolute densities of each resting morphotypes were fourth root
transformed. VEN = Vendicari pools (Sicily, Italy); TCL =
Torre Colimena (Vecchia Salina) pond (Apulia, Italy); NRT =
Nart saltworks (Vlor, Albania); KHE = Khersonesskoe lake
(Crimean Peninsula, Ukraine); KOY = Koyashskoe lake
(Crimean Peninsula, Ukraine).

Available information coming from the Vecchia Salina

[10] reported a total of 16 species in the water column
(deriving from a sampling effort which lasted over two
years). The number of cyst types (17) here reported from
the bottom sediments of the same environment is lower
than that (24) reported by the same authors, but in that
case the investigation was carried out on a total of 14 cores
collected in 14 different sites of the lake, while in the
present study only the central area of the lake was concerned by the collection of just 3 replicate cores.
It is evident that such a light sampling effort (3 sediment
cores at one sampling date) devoted to the sediments
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gives more information than a two-year period of sample

collection in the water. Nevertheless, we cannot ignore the
fact that some species do not supply the sediment cyst
bank but overcome adverse periods differently (e.g.
migrating as insects do, or resting as sub-adults, as some
harpacticoids do). Hence the analysis of cyst banks cannot
still completely substitute the traditional investigation on
active stages. It could be proposed, however, as an indispensable additional source of information to correctly
evaluate the biodiversity of water environments [10,13]. A
greater diversity of zooplankters are represented in the egg
banks in comparison to that present in the current water
column, these are dormant phases of the zooplankters life
cycle and favourable hatching conditions for those unique
cohorts may or may not occur within a given lake. The egg
banks stored in sediments of each lake represent its real
potential diversity. This does not diminish their importance over time because, as environmental conditions in a
lake change its appropriate zooplankter assemblage, it
will be more (or less) dominant.
As regards the species composition of each assemblage, it
can be noted that Koyashskoe and Nart were the poorest,
while Vendicari pools and Vecchia Salina saltworks were
the richest lakes.

Figure
thenogenetica
Best hatching
laboratory
Hexarthra
4 fennica
controlled
eggs;
patterns
eggs;
e) Moina
conditions:
of
c) Brachionus
some
salina
resting
a)
ephippia
Fabrea
sp.
stages
eggs;salina
d)
submitted
Artemia
cysts; b)
parto
Best hatching patterns of some resting stages submitted to laboratory controlled conditions: a) Fabrea
salina cysts; b) Hexarthra fennica eggs; c) Brachionus
sp. eggs; d) Artemia parthenogenetica eggs; e) Moina
salina ephippia. The values reported on the x-axis correspond to the storage time (in days); the y-axis represents the
hatching percentages.

Some information about salinity [see Additional file 3]

suggests that this could be due to the high salt concentrations characteristic of the first waters. The biodiversity of
saline habitats, in fact, seems to be inversely correlated
with the salinity value [1,15]. As regards the species composition, we can note that both the environments of Vendicari (Pantano Grande and Pantano Roveto) do not host
Artemia cysts, while they are the only habitats where diaptomid eggs have been found. As in the case described by
[16], despite the proximity to the sea, the salt is probably
not of marine but of athalassohaline origin (underground
brines). It has been proved that the quality of salt content
affects the biological community [6,7], and a chemical
analysis of dissolved anions in the Vendicari lakes water
will be the necessary future information to be collected to
confirm this rule. The sediments of both Vendicari lakes
(Pantano Grande and Pantano Roveto) sampled during
the dry season (September 2005), did not show the presence of Artemia cysts, while there have been recognized
eggs of other Anostraca (Phallocryptus sp.) and Calanoida
(Arctodiaptomus sp.). Although the two lakes are close to
the sea, this taxonomic composition of egg bank suggests
their salinity is not entirely of marine origin, but influenced by continental inputs.
The wide hatching patterns observed for most of the tested
species is thought to be an obligatory adaptation to the
extreme variability of the habitat. Hatching tests affirmed
that the 5 tested species inhabiting the present lakes dis-

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like freshwater conditions. Hatching has been found to be

highly variable, even among cysts coming from the same
sediment level, as well as among different layers of each
core, probably due to the need to spread the risk of non
successful hatching over many attempts, according to the
bet hedge theory of [17,18] to ensure the persistence of
populations in unpredictably stressed environments.
Indeed, most of cyst morphotypes here considered belong
to species that live in environments with a high level of
stochasticity [19], a condition in which bet-hedging is
expected to evolve [20].
Cyst banks form an essential component of plankton
ecology. As cyst banks integrate seasonal and year-to-year
variations in environmental conditions, they represent
the total species and genetic diversity in any community
better than the active component sampled at any one
time. Cyst banks can be considered the archive of the local
habitat, and overlooking the composition of the cyst bank
in the study of biodiversity and biogeography may result
in erroneous patterns and interpretations of the underlying processes.

Methods
Study site
The research interested, from April 2004 to September
2006, Khersonesskoe (4435'12"N; 3324'00"E) and
Koyashskoe (4502'31"N; 3612'20"E) lakes in the Crimea peninsula (Ukraine), Nart (4032'13"N;
1925'48"E) saltworks (Southern Albania), Vecchia
Salina (4018'06"N; 1743'56"E) at Torre Colimena
(Gulf of Taranto, Apulia, Italy), Pantano Grande and Pantano Roveto (3648'29"N; 1506'02"E) at Vendicari
Nature Reserve (Sicily, Italy) (Figure 5).

Collections of resting stages from the sediments of the 2

contiguous lakes at Vendicari (Sicily, Italy) allowed to
compare results coming from nearby habitats with those
coming from very distant ones (e.g. Italian and Crimean
lakes).
Sampling procedures
Samplings were collected during summer months corresponding to the minimum water level, or even its absence
to take only samples not submerged. Three replicate sediment cores (diameter, 7.5 cm; depth, 6 cm) were obtained
from each lake by using a core sampler (20 cm length) and
stored at 4C in a refrigerator for 1 year. For the analysis,
each sediment core was cut into 3 cm thick layers. Each
layer was ultrasonified to break the larger particles of sediment and then sieved at two mesh sizes (212 and 45 m).
The sediment collected by both sieves was centrifuged at
1,090 g in a 1:1 sucrose-distilled water solution for 3 min.
The supernatant derived from the centrifugation of the
two sieve fractions was analysed to separate cysts.

Figure
Geographical
ern
European
5
location
Region of the sampling sites in the South-EastGeographical location of the sampling sites in the
South-Eastern European Region. 1,2: Pantano Grande
and Pantano Roveto at Vendicari Nature Reserve (Italy); 3:
Vecchia Salina at Torre Colimena (Gulf of Taranto, Apulia,
Italy); 4: Nart saltworks (Albania); 5: Khersonesskoe lake (Crimea, Ucraine); 6: Koyashskoe lake (Crimea, Ucraine).
Cysts were reported as number per 100 cc of sediment.
The most abundant resting stages (2 types for the fraction
>212 m; 3 types for the fraction >45 m) were used in
hatch experiments in the laboratory. Sets of 30 cysts of
each morphotypes, taken from each layer (from the superficial to the deepest one), were stored in 3 cc wells raised
with 2 cc of original water filtered at 0,45 m. To avoid
bacterial growth, in each well, 20 l of an antibiotic mix
(streptomycin/penicillin 1:1) was added. Resting stages
were submitted to different storage conditions in thermostatic rooms (an "equinox" simulation, with 13C and 12
hL:12 hD photoperiod and a "early summer" simulation,
with 24C and 14 hL:10 hD photoperiod) at 4 different
salinity values (46, 36, 26, freshwater) obtained
by diluting the original-site water. Hatching plates were
checked daily to test the presence of active stages, which
were counted and removed for identification.
The related water column, on each lake, has been sampled
in different periods of the year (at least 2 seasons), and in
different years (between 2002 and 2006) to compare its
faunal composition to each other. Zooplankton samples
were collected monthly (three replicates), with two plankton nets (mouth diameter, 25 cm; length, 65 cm; mesh
size, 200 m and 50 m) towed horizontally, equipped
with a water-flow meter at the mouth. The Italian hypersaline lake Vecchia Salina and Crimean ones were already
studied in the past (see data in [10] and [16], respectively).
Data analysis
Data were analysed by multivariate statistical techniques
with a non-parametric approach because of the wide disparity in density of some cysts in different lakes. The sig-

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nificance of the spatial variation in "cyst banks"

composition was tested using a One-Way Analysis of Similarities for replicated data (ANOSIM) routine in PRIMER
(Plymouth Routines In Multivariate Ecological Research)
version 6 R6 (PRIMER-E) [21].

Additional file 2
Table S2. Cyst categories contributing most (80% cut off) to the biotic
characterisation of each lake (av.ab. = average abundance; av.sim. = average similarity; contrib.% = contribution percentage; cum.% = cumulative
percentage).
Click here for file
[http://www.biomedcentral.com/content/supplementary/17461448-5-3-S2.doc]

For multivariate analyses, the absolute densities of each

morphotypes were fourth root transformed, to severely
down-weight the importance of the very abundant species
so allowing the less dominant, and even the rare morphs,
to play some role in determining similarity among samples.
Stress values were shown for each MDS plot to indicate
the goodness of representation of differences among samples [22]. A One-Way similarity percentages procedure
(PRIMER SIMPER routine, Clarke [22]) was used in order
to obtain the percentage contribution that each taxon provided to Bray-Curtis similarities measures. A cut-off criterion was applied to allow the identification of a subset of
species whose cumulative percentage contribution
reached 80% of similarity value. SIMPER analysis consented to identify the species responsible for the biological characterisation of the "seed banks" stored in each
investigated lake.

Abbreviations

Additional file 3
Table S3. Hypersaline lakes considered in the present study (listed in longitudinal order): salinity () and depth (m) values.
Click here for file
[http://www.biomedcentral.com/content/supplementary/17461448-5-3-S3.doc]

Acknowledgements
This research was supported and gathers ideas produced in the framework
of the "Investigation of energy flows coupling to carbon cycle in hypersaline
lake/lagoon ecosystems for environmental management and new biotechnology development" INTAS Project.
The authors express their gratitude to E. Shesterina and N. Shadrin (IBSS,
Ukrainian Academy of Sciences, UKR), and to M. Shehu and B. Shkurtaj
(University of Vlor, AL) for inestimable assistance provided during the field
work.

VEN: Vendicari ponds; PGR: Pantano Grande; PRV: Pantano Roveto; TCL: Torre Colimena (Vecchia Salina) saltworks; NRT: Nart saltworks; KHE: Khersonesskoe lake;
KOY: Koyashskoe lake; hL: hours of light; hD: hours of
dark; sim%: similarity percentage.

References

Competing interests

4.
5.

The authors declare that they have no competing interests.

1.
2.
3.

6.

Authors' contributions
SM participated in the design of the study, executed cyst
collection in all the lakes, performed the statistical analysis and is responsible for the first draft of the manuscript.
GB conceived of the study, participated in its design and
coordinated all the steps, comprising the discussion of
results.

9.

Additional material

10.

Additional file 1
Table S1. Number of taxonomic groups representing the total biodiversity
(realised and potential) of the different lakes investigated.
Click here for file
[http://www.biomedcentral.com/content/supplementary/17461448-5-3-S1.doc]

7.

8.

11.
12.
13.
14.

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